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Fruitbody chemistry underlies the structure of endofungal bacterial communities across fungal guilds and phylogenetic groups

Abstract

Eukaryote-associated microbiomes vary across host taxa and environments but the key factors underlying their diversity and structure in fungi are still poorly understood. Here we determined the structure of bacterial communities in fungal fruitbodies in relation to the main chemical characteristics in ectomycorrhizal (EcM) and saprotrophic (SAP) mushrooms as well as in the surrounding soil. Our analyses revealed significant differences in the structure of endofungal bacterial communities across fungal phylogenetic groups and to a lesser extent across fungal guilds. These variations could be partly ascribed to differences in fruitbody chemistry, particularly the carbon-to-nitrogen ratio and pH. Fungal fruitbodies appear to represent nutrient-rich islands that derive their microbiome largely from the underlying continuous soil environment, with a larger overlap of operational taxonomic units observed between SAP fruitbodies and the surrounding soil, compared with EcM fungi. In addition, bacterial taxa involved in the decomposition of organic material were relatively more abundant in SAP fruitbodies, whereas those involved in release of minerals were relatively more enriched in EcM fruitbodies. Such contrasts in patterns and underlying processes of the microbiome structure between SAP and EcM fungi provide further evidence that bacteria can support the functional roles of these fungi in terrestrial ecosystems.

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Fig. 1: The relative abundance of bacterial taxa across fungal phylogenetic groups and functional guilds.
Fig. 2: Nonmetric multidimensional scaling (NMDS) ordination illustrating compositional differences in bacterial communities associated with different host taxa and functional guilds as well as their surrounding soils and different sample types.
Fig. 3: Patterns of bacterial diversity across fungal orders and functional guilds.
Fig. 4: The relationship between the chemical properties of soil and fungal fruitbodies.

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Acknowledgements

We thank Leho Tedersoo and three anonymous reviewers for constructive comments on the paper. We also thank Rasmus Puusepp for laboratory assistance. Funding was provided by Estonian Research Council grants (PUT1317 and IUT20-30), Swedish Research Council (Vetenskapsrådet, grant no: 2017‐05019) and the European Union through the European Regional Development Fund (the Center of Excellence EcolChange).

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MP, MB, and KP contributed to study design and writing; MP performed molecular and data analysis.

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Correspondence to Mari Pent or Mohammad Bahram.

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Pent, M., Bahram, M. & Põldmaa, K. Fruitbody chemistry underlies the structure of endofungal bacterial communities across fungal guilds and phylogenetic groups. ISME J 14, 2131–2141 (2020). https://doi.org/10.1038/s41396-020-0674-7

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